casereport herbaspirillum infection in humans: a case...
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Case ReportHerbaspirillum Infection in Humans: A Case Report andReview of Literature
Rashmi Dhital , Anish Paudel, Nidrit Bohra, and Ann K. Shin
Reading Hospital and Medical Center, Tower Health System, West Reading, PA, USA
Correspondence should be addressed to Rashmi Dhital; [email protected]
Received 5 December 2019; Revised 2 February 2020; Accepted 4 February 2020; Published 20 February 2020
Academic Editor: Raul Colodner
Copyright © 2020 Rashmi Dhital et al.&is is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Introduction. Herbaspirillum seropedicae are Gram-negative oxidase-positive nonfermenting rods of Betaproteobacteria class,commonly found in rhizosphere. More recently, some Herbaspirillium species have transitioned from environment to humanhosts, mostly as opportunistic (pathogenic) bacteria. We present a 58-year-old female with non-small-cell lung cancer (NSCLC)who presented with pneumonia and was found to have Herbaspirillum seropedicae bacteremia. Case History. A 58-year-oldwoman with NSCLC on Pralsetinib presented with fevers and rigors for 2 days. Coarse breath sounds were auscultated on the rightupper lung field. Labs revealed leukopenia andmild neutropenia. CTchest revealed right upper lobe pneumonia. She was admittedfor sepsis secondary to pneumonia and placed on broad spectrum antibiotics with intravenous piperacillin-tazobactam andvancomycin. &e patient continued to have fever 2 days after admission (max: 102.8°F). Preliminary blood cultures grew Gram-negative rods. &e patient continued to have temperature spikes on the 3rd day of antibiotics (Tmax 101.5°F). Blood culturesrevealed oxidase-positive nonfermenting rods. &e patient’s antibiotic was changed to IV meropenem on the 4th day of hos-pitalization. Ultimately, on the seventh day of hospitalization, the blood culture was confirmed from outside lab asHerbaspirillumseropedicae. &e patient started feeling better and defervesced after about 24 hours.Discussion. More recently,Herbaspirillum spp.have been recovered from humans. Our patient had Herbaspirillum bacteremia, and reported regularly cleaning her pond andweeding her garden with possible exposure to this environmental proteobacterium. Herbaspirillum may be more prevalent thanearlier thought owing to misidentification. With the institution of appropriate antimicrobial therapy, the outcomes seemmostly favorable.
1. Introduction
Herbaspirillum seropedicae are Gram-negative oxidase-positive nonfermenting rods of Betaproteobacteria class,commonly found in the rhizosphere of maize and rice,which promote plant growth via biological nitrogen fixa-tion and phytohormone production [1, 2]. More recently,some Herbaspirillium species have transitioned from en-vironment (water, contaminated soil, plant internal tissues,and root nodules) to human hosts, mostly as opportunistic(pathogenic) bacteria. Cases of human colonization andinfection have mostly been noted in cystic fibrosis andimmunocompromised cancer patients [3–8] and also insome patients without an apparent immunosuppressedstate [9–11].
1.1. Case History. A 58-year-old woman with a medicalhistory of non-small-cell lung cancer (NSCLC) with ma-lignant left pleural effusion (with RETmutation under phase1 trial with pralsetinib), nonbacterial thrombotic endo-carditis, and pulmonary embolism presented to the hospitalwith fevers, chills, and rigors for 2 days. At presentation, shewas febrile with a temperature of 101 F and tachycardic at114 beats/minute. Physical examination revealed a Port-A-catheter on the right upper chest. Coarse breath sounds wereauscultated on the right upper lung field. Labs revealedanemia with the hemoglobin level of 6.4 (ref: 12.0–16.0 g/dl),leukopenia with the white blood cell (WBC) count of 1.7 (ref4.8–10.8 10E3/ul), mild neutropenia with the absoluteneutrophil count (ANC) of 1353 cells per microliter, anelevated C-reactive protein (CRP) level of 22.52 (ref range
HindawiCase Reports in Infectious DiseasesVolume 2020, Article ID 9545243, 6 pageshttps://doi.org/10.1155/2020/9545243
<1.00) mg/dl, and an elevated creatinine level of 1.56mg/dl(baseline creatinine of 1mg/dl). CT chest revealed rightupper lobe pneumonia, scattered small pulmonary nodulesconsistent with metastatic disease, and stable bony meta-static disease of the anterior left 6th rib. She was admitted forsepsis secondary to pneumonia and placed on broad spec-trum antibiotics with intravenous piperacillin-tazobactamand vancomycin. She received 2 units of packed red celltransfusion with stable hemoglobin thereafter. Urine anal-ysis was unremarkable. Urine legionella and streptococcuspneumonia antigens were negative.
&e patient continued to have fever 2 days after admission(max: 102.8 F). Preliminary blood cultures done at our hos-pital at Day 2 of hospitalization revealed Gram-negative rods.CT abdomen and pelvis revealed small volume of ascites andjejunal wall thickening with mild adjacent mesenteric edema,suggestive of enteritis. CT chest revealed persistent rightupper lobe pneumonia. &e patient continued to have tem-perature spikes on the 3rd day of antibiotics (Tmax 101.5 F).Blood cultures revealed oxidase-positive nonfermenting rods.&e organism was not clearly identified in our lab, and thespecimen was sent to Central Pennsylvania Alliance Labo-ratory for identification by DNA sequencing using MALDI(matrix-assisted laser desorption/ionization) technique. &epatient’s antibiotic was changed to IV meropenem on the 4thday of hospitalization. Port was removed and catheter tipculture was sent, which came out to be negative.
Ultimately, on the seventh day of hospitalization, theblood culture was identified from outside lab as Herbas-pirillum seropedicae (which was susceptible to all testedantibiotics including amikacin, cefepime, ceftazidime,ciprofloxacin, aztreonam, levofloxacin, meropenem, piper-acillin/tazobactam, and ticarcillin/clavulanate). &e patientstarted feeling better and defervesced after about 24 hours ofbeing on meropenem. &e patient was discharged with amidline catheter to continue IV meropenem for a total of 14days and follow-up for outpatient monitoring. &e WBCcount at discharge was 5.1× 10 µ/L, ANC was 3978 cells/microliter, and CRP was 6.36mg/dl. On further questioningto assess for risk factors, the patient reported taking care ofher pond and regularly cleaning weeds.
2. Discussion
&e first described species of the genus Herbaspirillum wasthe bacterium Herbaspirillum seropedicae, which was foundcolonizing the roots and aerial parts of important crops [1].More recently, Herbaspirillum spp. have been recoveredfrom the blood and sputum/bronchoalveolar lavage of pa-tients with cystic fibrosis and pneumonia [4, 6, 11] and fromblood in patients with leukemia [6, 7, 12], aplastic anemia[7], multiple myeloma [13], and cellulitis [8]. Our patient is a58-year-old woman with NSCLC on RET-inhibitor pralse-tinib who presented with right upper lobe pneumonia andhad blood culture positive for oxidase-positive non-fermenting Gram-negative rod, which was confirmed asHerbaspirillium only on Day 7 of hospitalization by whichtime the patient was already improving with meropenemtherapy. On retrospect, our patient had been regularly
cleaning her pond and weeding her garden with possibleexposure to this environmental proteobacterium, support-ing this change in dynamics from environmental bacteriumto opportunistic pathogen. However, it is not entirely clearwhy the patient only defervesced and improved after 24hours of switching piperacillin/tazobactam to meropenem,even though her culture report suggested sensitivity topiperacillin/tazobactam. New genomic data findings suggestthat the transition from environmental to pathogenic led tothe loss and acquisition of specific genes to allow coloni-zation and survival in new environments. &e strains thathave been infectious to humans have lost the genes fornitrogen fixation and acquired genes for lipopolysaccharidebiosynthesis with the addition of sialic acids to evade theimmune system [1].
We reviewed the literature for available Herbaspirillumcases and identified 9 published studies from 2005 to 2019(Table 1), with Herbaspirillum bacteremia, cellulitis orpneumonia. Tan and Oehler reported Herbaspirillum bac-teremia and cellulitis in a patient with aquatic exposure [8].Ziga et al. reported Herbaspirillum bacteremia in a 2-year-old girl with a history of acute lymphoblastic leukemia (ALL)after induction chemotherapy and stem cell transplant [6].Chen et al. reported Herbaspirillum bacteremia in an ALLpatient on chemotherapy after taking sugarcane juice [12].Regunath et al. described a case of bacteremia caused bygentamicin-resistant Herbaspirillum in an immunocompe-tent adult male farmer [11]. Suwantarat et al. reported thefirst fatal case-related H. seropedicae bacteremia secondaryto pneumonia in an immunocompromised 65-year-old manwith end-stage renal disease and multiple myeloma [13].Abreu-Di Berardino et al. described Herbaspirillum hut-tiense pneumonia in a patient with essential thrombocytosis[9]. Liu et al. reported Herbaspirillum huttiense bacteremiain an elderly patient with no obvious immune suppression,who later went on to develop a pneumonia, where despiteadequate treatment, microbiological eradication was noteasily achieved, and septicemia lasted for several days alongwith sputum culture positivity forHerbaspirillum huttiense 2months later [10].
Chemaly et al. investigated a potential cluster of hospital-based Herbaspirillum infections in cancer patients at theUniversity of Texas MD Anderson Cancer Center, initiallyidentified as Burkholderia cepacia complex and subsequentlyreidentified as Herbaspirillum species by the Cystic FibrosisFoundation Burkholderia cepacia Research Laboratory andRepository (BcRLR) at the University of Michigan. &eauthors identified a total of 8 patients with bacteremia andpneumonia with cultures positive for Herbaspirillum speciesbetween July 2011 and August 2012 (including 5 clusters and3 additional cases identified prospectively). 5 of the 8 pa-tients were females and the median age was 53 years (2–67years) [7].
Spilker et al. reported a 26-year-old male with moderateto severe lung disease with Gram-negative rod bacteremia athospital day 23. &e patient was admitted for methicillin-resistant staphylococcus aureus (MRSA) and Pseudomonaspneumonia, and cultures were initially misidentified asBurkholderia cepacia complex [4]. &e authors analyzed
2 Case Reports in Infectious Diseases
Tabl
e1:
Summarytableof
publish
edcasesof
Herbaspirillu
minfectionin
humans.
Autho
ryear,
coun
try
Age/
sex
Past
history/
predisp
osing
cond
ition
s/cancer/
HCST
Immun
esupp
ression
Likely
risk
factor/in
citin
gevent
Reason
for
admiss
ion/Clin
ical
presentatio
nInitial
antib
iotics
Respon
seto
initial
antib
iotics/
subsequent
antib
iotics
Specim
ensource
positivefor
Herbaspirillu
m
Liu2019,K
orea
93/F
Hypertension
Advancedage
N/A
—
(i)Fever,seizure
(ii)A
ftera
fewdays,
hypo
xiaandchest
X-ray
with
pneumon
ia
Empiric
vancom
ycin+ceftriaxone
for
enceph
alitis
Chang
edto
merop
enem
and
colistin
at10
days
and
changedto
cefta
zidime,
minocyclin
e,and
trim
etho
prim
/sulfametho
xazole
thereafte
r
Bloo
d:Herbaspirillu
mhu
ttiense
2mon
thslater,
sputum
:Herbaspirillu
mhu
ttiense
Abreu-di
berardino2019,
Spain
59/F
Aortic
wall
thrombo
sis,v
isceral
andcerebral
ischemic
lesio
ns,
JAK2+essential
thrombo
cytopenia,
new
DM
N/A
—
(i)Generalized
decond
ition
ing
(ii)D
yspn
ea10
days
afteradmiss
ion,
nosocomial
pneumon
ia
Piperacillin-tazobactam
Recoveredcompletely
afterantib
iotics
Sputum
:Herbaspirillu
mhu
ttiense
Chen2010,C
hina
48/F
Acute
lymph
oblastic
leuk
emia
On
chem
otherapy
andG-C
SF
Drank
sugarcanejuice
before
fever
started
Fever,chills
Cefmetazoleandgatifl
oxacin
Improved
Bloo
d:Herbaspirillu
mhu
ttiense
Spilk
er2008,U
SA26/
m
Mod
erateto
severe
lung
disease,
pancreatic
insufficiency,
diabetes,a
ndliver
disease
Recent
multip
leadmiss
ions
for
exacerbatio
nof
respiratory
symptom
s
—
Fevers
andrigors,
MRS
A,and
Pseudomon
asaerugino
sabacterem
ia
Vancomycin,p
iperacillin-
tazobactam
,and
tobram
yicn
x20
days
Antibiotic
discon
tinuedat20
days,afte
rFE
V1startedto
improve
Ontheho
spita
lday
23:fever
andrigors
Chang
edto
intravenou
scefta
zidimeand
tobram
ycin
andoral
trim
etho
prim
-sulfametho
xazole
(TMP-SM
X),
levoflo
xacin,
and
minocyclin
e
Bloo
d:(G
NR,
initially
identifi
edas
burkholderia
cepacia
complex)Later,
identifi
edas
Herbaspirillu
mspecies
Case Reports in Infectious Diseases 3
Tabl
e1:
Con
tinued.
Autho
ryear,
coun
try
Age/
sex
Past
history/
predisp
osing
cond
ition
s/cancer/
HCST
Immun
esupp
ression
Likely
risk
factor/in
citin
gevent
Reason
for
admiss
ion/Clin
ical
presentatio
nInitial
antib
iotics
Respon
seto
initial
antib
iotics/
subsequent
antib
iotics
Specim
ensource
positivefor
Herbaspirillu
m
Tan2005,U
SA49/
mProb
able
hepatic
cirrho
sis—
Hom
eless
Jumpedfrom
abridge
into
afreshw
ater
canalincentral
Florida
Increasin
gerythemaand
warmth
totheleft
leg(cellulitis)
Ampicillin/sulbactam
Antibioticssw
itched
tocefepimeand
levoflo
xacinafter
initial
bloo
dcultu
reresults
Bloo
d:(oxidase-
positiveno
nlactose-
ferm
entin
gGNR,subm
itted
toan
outsidereference
labo
ratory)po
sitive
forHerbaspirillu
mseropedicae
Regunath
2014,
USA
46/
M
Childho
odasthma,
atypicalpn
eumon
iaas
ateenager,
tonsillectomy
N/A
Farm
ingin
ruralM
issou
ri,
closecontact
with
cattleand
turkeys,mold
andpo
ssible
rat
excreta
Drenchedin
rain
during
afishing
trip
Fever,fatig
ue,S
OB,
nigh
tsweats,
anorexia,m
yalgia,
andheadache
Dry
cough,
righ
t-sid
edpleuritic
chestp
ain,
andworsening
dyspneaHypoxia
(multilob
arpn
eumon
ia)
Vancomycin,ceftriaxone,
andazith
romycin
Ceftriaxone
switched
topiperacillin-
tazobactam
Azithromycin
switchedto
Doxycyclin
eAfte
r12
days
oftreatm
ent,thepatient
improved
andwas
extubated
Bloo
d(D
ay1)
(from
referringfacility)
identifi
edas
Burkholderia
cepacia
complex
(BCC),later
asHerbaspirillu
maqua
ticum
orHerbaspirillu
mhu
ttiense
BAL(D
ay3):G
NRas
Herbaspirillu
maqua
ticum
orHerbaspirillu
mhu
ttiense
Chemaly2015,
USA
Hospital-b
ased
clusterof
Herbaspirillium
spinfections
initially
misidentified
asB.
cepacia
48/F
Ovarian
adenocarcino
ma
Chemotherapy
Source
and
mechanism
ofthecluster
unkn
own
Pseudo
mon
asBS
I,sepsis-CRB
SI
Cefepim
e(5
patients),
cefta
zidime(1
patient),
moxifloxacin
(1patient),
merop
enem
(1patient)
initially
Follo
wed
byceftriaxone
orflu
oroq
uino
lone
Allpatientsim
proved
with
antib
iotic
and
hadnegativ
erepeat
bloo
dcultu
res
1patient
had
recurrence,w
hich
resolved
once
thepo
rtwas
removed
Bloo
d,Infusapo
rttip
67/F
Leuk
emia
Chemotherapy
MRS
Apn
eumon
ia,
sepsis-BS
IBloo
d
58/
MLeuk
emia/H
SCT
High-do
sesteroid
GIbleedGVHD,
BSI
Bloo
d
55/F
Leuk
emia/H
SCT
High-do
sesteroid
GIGVHD,B
SIBloo
d
2/M
Ependymom
aHigh-do
sesteroid
Herbaspirillium
Sepsis-BS
IBloo
d
4 Case Reports in Infectious Diseases
Tabl
e1:
Con
tinued.
Autho
ryear,
coun
try
Age/
sex
Past
history/
predisp
osing
cond
ition
s/cancer/
HCST
Immun
esupp
ression
Likely
risk
factor/in
citin
gevent
Reason
for
admiss
ion/Clin
ical
presentatio
nInitial
antib
iotics
Respon
seto
initial
antib
iotics/
subsequent
antib
iotics
Specim
ensource
positivefor
Herbaspirillu
m
3additio
nal
Herbaspirillium
spaftercontinued
surveillance
(sporadic)
66/F
Historyof
recurrent
pneumon
ia,lun
gcancer
Radiation
therapy
Herbaspirillium
Sepsis-pn
eumon
iaSputum
18/
MLymph
oma
Chemotherapy
Chemotherapy
Sepsis-BS
IBloo
d
51/F
Aplastic
anem
ia/
HSC
TTacrolim
usHerbaspirillium
Sepsis-
CRB
SIBloo
d,PICClin
etip
Suwantarat2015,
USA
65/
M
Multip
lemyeloma
ESRD
onhemod
ialysis
Steroids
and
lenalid
omide
Acute
respiratory
failu
reandseptic
shockRigh
tlow
erlobe
pneumon
ia
Vancomycin,cefepim
e,ciprofl
oxacin,and
micafun
gin
Chang
edto
vancom
ycin,
merop
enem
,and
gentam
icin
with
in12
hoursHow
ever,the
patient
remained
clinicallyun
stableand
died
after4days
BAL(oxidase-
positive,no
nlactose-
ferm
entin
gGNR),
initially
identifi
edas
Cupriavidu
s,lateras
Herbaspirillu
mBloo
d:Herbaspirillu
mseropedicae
Ziga
2010,U
SA2/F
Acute
lymph
oblastic
leuk
emia
Chemotherapy,
HSC
T
Uncertain
Lives
with
herp
arents
and
grandp
arents
onalargefarm
Feveranddiarrhea
Cefepim
e
Gentamicin
added
afteroxidase-po
sitive,
weaklycatalase-
positive,Gram-
negativ
ebacillu
sLater,sw
itchedto
merop
enem
Bloo
dBu
rkholderia
cepaciacomplex
As
susceptib
ilitypatte
rnwas
notc
onsis
tent,
furtheridentificatio
nwas
pursued:
Herbaspirillu
msp
G-C
SF:g
ranu
locyte-colon
ystim
ulatingfactor;B
AL:
bron
choalveolarlavage;G
IGVHD:g
astrointestin
algraftv
ersusho
stdisease;BS
I:bloo
dstream
infection;
CRB
SI:catheter-relatedbloo
dstream
infection;
HSC
T:hematop
oietic
stem
cellinfection;
GNR:
gram
-negativerod.
Case Reports in Infectious Diseases 5
isolates from sputum from over 1,100 cystic fibrosis patientsacross 8 years (January 2000 to December 2007) and foundHerbaspirillum in only 28 patients (<3%) with ages rangingfrom 20 months to 5 years, of which 3 isolates were Her-baspirillum huttiense, 3 were Herbaspirillum frisingense, 2were Herbaspirillum seropedicae, and 2 were Herbaspirillumputei, and the remaining eighteen isolates could not bespeciated [4]. Prior to the correct identification of Herbas-pirillum at the BcRLR for the above 28 specimen, they hadbeen identified as Burkholderia cepacia complex in 19 (68%)and Ralstonia in 4 (14%).Most patients appeared to have hadtransient respiratory tract colonization with Herbaspirillumexcept for bacteremia in one patient and a chronic respi-ratory tract infection in another [4].
Tetz and Tetz, for the first time, identifiedHerbaspirillumfrisingense from the bladder of a human patient with urinarytract infection (UTI). Furthermore, genome analysisrevealed numerous factors such as adhesins, urease, he-molysin D, and pilin that contribute to the bacterium’svirulence in UTIs. &e authors suggested that further re-search of this Herbaspirillum spp would aid in better un-derstanding of its implication in UTI [14]. Similarly, Wuet al. performed a comprehensive analysis of urinary mi-croenvironment of bladder cancer and identified Herbas-pirillum as one of the species associated with an increasedrisk of progression, suggesting its potential role in riskstratifying bladder cancer [15].
As evidenced by the above studies, Herbaspirillum is anemerging pathogen and may be more prevalent than earlierthought owing to misidentification for organisms likeBurkholderia cepacia complex due to phylogenetic andphenotypic resemblance [4, 6, 7, 13]. Antimicrobial sus-ceptibilities may serve as a means for differentiating Her-baspirillum species from Burkholderia cepacia complexbecause the latter are usually multidrug resistant, whereasHerbaspirillum is not. With the institution of appropriateantimicrobial therapy, the outcomes seem mostly favorableand the bacteria appear to be easily eradicated, except in 1case reported by Liu et al. Misidentification as Burkholderiacomplex can have serious implications for clinical care, anddistinction between these is important due to different re-sistance profiles and different therapeutic implications. &eincreased availability of newer molecular methods (e.g.,MALDI-TOF MS) should allow laboratories to correctlyidentify this organism and reduce misidentification byestablished microbial identification systems.
Conflicts of Interest
&e authors declare that they have no conflicts of interest.
References
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6 Case Reports in Infectious Diseases